The hydrogen exchange core and protein folding

Protein Science

Volumn 8, Issue 8, 1999, Pages 1571-1590

  Renhao, Li ^a   Woodward, Clare ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Hydrogen exchange; NMR; Protein folding; Slow exchange core

Indexed keywords

AMIDE; DEUTERIUM;

ENERGY; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTON TRANSPORT; REVIEW;

BOVINAE; LEPUS;

EID: 0344603844     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.8.8.1571     Document Type: Review

References (126)

1. Alonso DO, Daggett V. 1995. Molecular dynamics simulations of protein unfolding and limited refolding: Characterization of partially unfolded states of ubiquitin in 60% methanol and in water. J Mol Biol 247:501-520.
2. Anderson DE, Lu J, McIntosh L, Dahlquist FW. 1993. T4 lysozyme. In: Clore GM, Gronenborn AM, eds. NMR of proteins. Boca Raton: CRC Press. pp 258-304.
3. Arcus VL, Vuilleumier S, Freund SM, Bycroft M, Fersht AR. 1995. A comparison of the pH, urea, and temperature-denatured states of barnase by heteronuclear NMR: Implications for the initiation of protein folding. J Mol Biol 254:305-321.
4. Arlington C, Teesch L, Robertson A. 1999. Defining protein ensembles with native-state NH exchange: Kinetics of interconversion and cooperative units from combined NMR and MS analysis. J Mol Biol 285:1265-1275.
5. Arlington CB, Robertson AD. 1997. Microsecond protein folding kinetics from native-state hydrogen exchange. Biochemistry 56:8686-8691.
6. Bai Y, Karimi A, Dyson HJ, Wright PE. 1997. Absence of a stable intermediate on the folding pathway of protein A. Protein Sci 6:1449-1457.
7. Bai Y, Milne JS, Mayne L, Englander SW. 1993. Primary structure effects on peptide group hydrogen exchange. Proteins Struct Funct Genet 17:75-86.
8. Barbar E, Barany G, Woodward C. 1995. Dynamic structure of a highly ordered β-sheet molten globule: Multiple conformations with a stable core. Biochemistry 34:11423-11434.
9. Barbar E, Hare M, Daragan V, Barany G, Woodward C. 1998. Dynamics of the conformational ensemble of partially folded bovine pancreatic trypsin inhibitor. Biochemistry 37:7822-7833.
10. Bond CJ, Wong K-B, Clarke J, Fersht AR, Daggett V. 1997. Characterization of residual structure in the thermally denatured state of barnase by simulation and experiment: Description of the folding pathway. Proc Natl Acad Sci USA 94:13409-13413.
11. Bowie JU, Reidhaar-Olson JF, Lim WA, Sauer RT. 1990. Deciphering the message in protein sequences: Tolerance to amino acid substitutions. Science 247:1306-1310.
12. Briggs MS, Roder H. 1992. Early hydrogen-bonding events in the folding reaction of ubiquitin. Proc Natl Acad Sci USA 59:2017-2021.
13. Buck M, Radford SE, Dobson CM. 1993. A partially folded state of hen egg white lysozyme in trifluoroethanol: Structural characterization and implications for protein folding. Biochemistry 32:669-678.
14. Buck M, Radford SE, Dobson CM. 1994. Amide hydrogen exchange in a highly denatured state. Hen egg-white lysozyme in urea. J Mol Biol 237:247-254.
15. Burton RE, Huang GS, Daugherty MA, Calderone TL, Oas TG. 1997. The energy landscape of a fast-folding protein mapped by Ala → Gly substitutions. Nat Struct Biol 4:305-310.
16. Bycroft M, Matouschek A, Kellis JT Jr, Serrano L, Fersht AR. 1990. Detection and characterization of a folding intermediate in barnase by NMR. Nature 340:488-490.
17. Chamberlain AK, Handel TM, Marqusee S. 1996. Detection of rare partially folded molecules in equilibrium with the native conformation of RNase H. Nat Struct Biol 3:782-787.
18. Chung EW, Nettleton EJ, Morgan CJ, Gross M, Miranker A, Radford SE, Dobson CM, Robinson CV. 1997. Hydrogen exchange properties of proteins in native and denatured states monitored by mass spectrometry and NMR. Protein Sci 6:1316-1324.
19. Chyan CL, Wormald C, Dobson CM, Evans PA. Baum J. 1993. Structure and stability of the molten globule state of guinea-pig α-lactalbumin: A hydrogen exchange study. Biochemistry 32:5861-5891.
20. Clarke J, Fersht AR. 1996. An evaluation of the use of hydrogen exchange at equilibrium to probe intermediates on the protein folding pathway. Folding Design 1:243-254.
21. Clarke J, Itzhaki LS, Fersht AR. 1997. Hydrogen exchange at equilibrium: A short cut for analysing protein-folding pathways? Trends Biochem Sci 22:284-287.
22. Dabora JM, Pelton JG, Marqusee S. 1996. Structure of the acid state of Escherichia coli ribonuclease HI. Biochemistry 35:11951-11958.
23. Daggett V, Li A, Itzhaki LS, Otzen DE, Fersht AR. 1996. Structure of the transition state for folding of a protein derived from experiment and simulation. J Mol Biol 257:430-440.
24. Deng Y, Smith DL. 1998. Identification of unfolding domains in large proteins by their unfolding rates. Biochemistry 37:6256-6262.
25. Dill KA, Chan HS. 1997. From Levinthal to pathways to funnels. Nat Struct Biol 4:10-19.
26. 1H NMR spectroscopy. Biochemistry 29:4668-4682.
27. Elöve GA, Bhuyan AK, Roder H. 1994. Kinetic mechanism of cytochrome c folding: Involvement of the heme and its ligands. Biochemistry 33:6925-6935.
28. Englander SW. 1998. Native-state HX. Trends Biochem Sci 23:378.
29. Englander SW, Kallenbach NR. 1984. Hydrogen exchange and structural dynamics of proteins and nucleic acids. Q Rev Biophys 16:521-655.
30. Englander SW, Mayne L. 1992. Protein folding studied using hydrogen-exchange labeling and two-dimensional NMR. Ann Rev Biophys Biomol Struct 21:243-265.
31. Fan P, Bracken C, Baum J. 1993. Structural characterization of monellin in the alcohol-denatured state by NMR: Evidence for β-sheet to α-helix conversion. Biochemistry 32:1573-1582.
32. Fersht AR. 1998. A reply to Englander and Woodward. Trends Biochem Sci 23:379-381.
33. Fersht AR. 1993. Protein folding and stability: The pathway of folding of barnase. FEBS Lett 325:5-16.
34. Fersht AR, Matouschek A, Serrano L. 1992. The folding of an enzyme I. Theory of protein engineering analysis of stability and pathway of protein folding. J Mol Biol 224:771-782.
35. Freund C, Gehrig P, Holak TA, Plückthun A. 1997. Comparison of the amide proton exchange behavior of the rapidly formed folding intermediate and the native state of an antibody scFv fragment. FEBS Lett 407:42-46.
36. Freund C, Honegger A. Hunziker P, Holak TA, Plückthun A. 1996. Folding nuclei of the scFv fragment of an antibody. Biochemistry 35:8457-8464.
37. Gassner NC, Baase WA, Matthews BW. 1996. A test of the jigsaw puzzle model for protein folding by multiple methionine substitutions within the core of T4 lysozyme. Proc Natl Acad Sci USA 93:12155-12158.
38. Gladwin ST, Evans PA. 1997. Structure of very early protein folding intermediates: New insights through a variant of hydrogen exchange labelling. Folding Design 1:407-417.
39. Grantcharova VP, Baker D. 1997. Folding dynamics of the src SH3 domain. Biochemistry 36:15685-15692.
40. Grantcharova VP, Riddles DS, Santiago JV, Baker D. 1998. Important role of hydrogen bonds in the structurally polarized transition state for folding of the src SH3 domain. Nat Struct Biol 5:714-720.
41. Gregory RB, Dinh A, Rosenberg A. 1986. The effect of Tri-N-acetylglucosamine on hydrogen exchange in hen egg white lysozyme. J Biol Chem 261:13963-13968.
42. Gu H, Kim D, Baker D. 1997. Contrasting roles for symmetrically disposed β-turns in the folding of a small protein. J Mol Biol 274:588-596.
43. Hamada D, Goto Y. 1997. The equilibrium intermediate of β-lactoglobulin with non-native a-helical structure. J Mol Biol 269:479-487.
44. Harding MM, Williams DH, Woolfson DN. 1991. Characterization of a partially denatured state of a protein by two-dimensional NMR: Reduction of the hydrophobic interactions in ubiquitin. Biochemistry 30:3120-3128.
45. Hilser VJ, Dowdy D, Oas TG, Freire E. 1998. The structural distribution of cooperative interactions in proteins: Analysis of the native state ensemble. Proc Natl Acad Sci USA 95:9903-9908.
46. Hilton BD, Trudeau K, Woodward CK. 1981. Hydrogen exchange rates in pancreatic trypsin inhibitor are not correlated to thermal stability in urea. Biochemistry 20:4697-4703.
47. Holm L, Sander C. 1998. Touring protein fold space with Dali/FSSP. Nucleic Acids Res 26:316-319.
48. Hughson FM, Wright PE, Baldwin RL. 1990. Structure characterization of a partly folded apomyoglobin intermediate. Science 249:1544-1548.
49. Hvidt A, Nielsen SO. 1966. Hydrogen exchange in proteins. Adv Protein Chem 21:288-386.
50. Itzhaki LS, Neira JL, Fersht AR. 1997. Hydrogen exchange in chymotrypsin inhibitor 2 probed by denaturants and temperature. J Mol Biol 270:89-98.
51. Itzhaki LS, Otzen DE, Fersht AR. 1995. The structure of the transition state for folding of chymotrypsin inhibitor 2 analysed by protein engineering methods: Evidence for a nucleation-condensation mechanism for protein folding. J Mol Biol 254:260-288.
52. Jackson SE, elMasry N, Fersht AR. 1993. Structure of the hydrophobic core in the transition state for folding of chymotrypsin inhibitor 2: A critical test of the protein engineering method of analysis. Biochemistry 32:11270-11278.
53. Jacobs MD, Fox RO. 1994. Staphylococcal nuclease folding intermediate characterized by hydrogen exchange and NMR spectroscopy. Proc Natl Acad Sci USA 91:449-453.
54. Jeng M, Englander SW, Elöve GA, Wand AJ, Roder H. 1990. Structural description of acid-denatured cytochrome c by hydrogen exchange and 2D NMR. Biochemistry 29:10433-10437.
55. Jennings PA, Wright PE. 1993. Formation of a molten globule intermediate early in the kinetic folding pathway of apomyoglobin. Science 262:892-896.
56. Karplus M. 1997. The Levinthal paradox: Yesterday and today. Folding Design 2:S69-S75.
57. Kim KS, Fuchs JA, Woodward CK. 1993. Hydrogen exchange identifies native-state motional domains important in protein folding. Biochemistry 32:9600-9608.
58. Kim KS, Woodward C. 1993. Protein internal flexibility and global stability: Effect of urea on hydrogen exchange rates of bovine pancreatic trypsin inhibitor. Biochemistry 32:9609-9613.
59. Kraulis PJ. 1991. MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr 24:946-950.
60. Kuszewski J, Clore GM, Gronenborn AM. 1994. Fast folding of a prototypic polypeptide: The immunoglobulin binding domain of streptococcal protein G. Protein Sci 3:1945-1952.
61. Kuwajima K. 1989. The molten globule state as a clue for understanding the folding and cooperativity of globular-protein structure. Proteins Struct Funct Genet 6:87-103.
62. Kuwajima K. 1996. The molten globule state of α-lactalbumin. FASEB J 10:102-109.
63. Lacroix E, Bruix M, López-Hernández E, Serrano L, Rico M. 1997. Amide hydrogen exchange and internal dynamics in the chemotactic protein Che Y from Escherichia coli. J Mol Biol 271:472-487.
64. Lazaridis T, Karplus M. 1997. "New view" of protein folding reconciled with the old through multiple unfolding simulations. Science 278:1928-1931.
65. Loh SN, Kay MS, Baldwin RL. 1995. Structure and stability of a second molten globule intermediate in the apomyoglobin folding pathway. Proc Natl Acad Sci USA 92:5446-5450.
66. Loh SN, Prehoda KE, Wang J, Markley JL. 1993. Hydrogen exchange in unligated and ligated staphylococcal nuclease. Biochemistry 32:11022-11028.
67. López-Hernández E, Serrano L. 1996. Structure of the transition state for folding of the 129 aa protein Che Y resembles that of a smaller protein, CI-2. Folding Design 1:43-55.
68. Lu J, Dahlquist FW. 1992. Detection and characterization of an early folding intermediate of T4 lysozyme using pulsed hydrogen exchange and two-dimensional NMR. Biochemistry 31:4749-4156.
69. Lumry R. 1991. A study of enzymes, Volume 2. In: Kuby SA, ed. Mechanism of enzyme action. Boca Raton: CRC Press. pp 3-81.
70. Lumry R. 1995. On the interpretation of data from isothermal processes. Methods Enzymol 259:628-720.
71. Lumry R, Rosenberg A. 1975. The mobile defect hypothesis of protein function. Col Int CNRS L'Eau Syst Biol 246:55-63.
72. Matagne A, Chung EW, Ball LJ, Radford SE, Robinson CV, Dobson CM. 1998. The origin of the α-domain intermediate in the folding of hen lysozyme. J Mol Biol 277:997-1005.
73. 2H exchange-nuclear magnetic resonance studies on the folding pathway of barnase: Complementarity to and agreement with protein engineering studies. J Mol Biol 224:837-845.
74. Miller DW, Dill KA. 1995. A statistical mechanical model for hydrogen exchange in globular proteins. Protein Sci 4:1860-1873.
75. Miranker A, Radford SE, Karplus M, Dobson CM. 1991. Demonstration by NMR of folding domains in lysozyme. Nature 349:633-636.
76. Montelione GT, Anderson S. 1999. Structural genomics: Keystone for a human proteome project. Nature Struct Biol 6:11-12.
77. Mori S, van Zijl PC, Shortle D. 1997. Measurement of water-amide proton exchange rates in the denatured state of staphylococcal nuclease by a magnetization transfer technique. Proteins Struct Funct Genet 28:325-332.
78. Morozova LA, Haynie DT, Arico-Muendel C, Van Dael H, Dobson CM. 1995. Structural basis of the stability of a lysozyme molten globule. Nature Struct Biol 2:871-875.
79. Morozova-Roche LA, Arico-Muendel CC, Haynie DT, Emelyanenko VI, Van Dael H, Dobson CM. 1997. Structural characterisation and comparison of the native and A-states of equine lysozyme. J Mol Biol 268:903-921.
80. Mullins LS, Pace CN, Raushel FM. 1993. Investigation of ribonuclease T1 folding intermediates by hydrogen-deuterium amide exchange - Two-dimensional NMR spectroscopy. Biochemistry 32:6152-6156.
81. Mullins LS, Pace CN, Raushel FM. 1997. Conformational stability of ribonuclease TI determined by hydrogen-deuterium exchange. Protein Sci 6:1387-1395.
82. Nash D, Lee BS, Jonas J. 1996. Hydrogen-exchange kinetics in the cold denatured state of ribonuclease A. Biochim Biophys Acta 1297:40-48.
83. Nash DP, Jonas J. 1997. Structure of pressure-assisted cold denatured lysozyme and comparison with lysozyme folding intermediates. Biochemistry 36:14375-14383.
84. Neira JL, Itzhaki LS, Otzen DE, Davis B, Fersht AR. 1997. Hydrogen exchange in chymotrypsin inhibitor 2 probed by mutagenesis. J Mol Biol 270:99-110.
85. Onuchic JN, Luthey-Schulten Z, Wolynes PG. 1997. Theory of protein folding: The energy landscape perspective. Ann Rev Phys Chem 48:545-600.
86. Orban J, Alexander P, Bryan P, Khare D. 1995. Assessment of stability differences in the protein G B1 and B2 domains from hydrogen-deuterium exchange: Comparison with calorimetric data. Biochemistry 34:15291-15300.
87. Pan H, Barbar E, Barany G, Woodward C. 1995. Extensive non-random structure in reduced and unfolded bovine pancreatic trypsin inhibitor. Biochemistry 34:13974-13981.
88. Pan Y, Briggs MS. 1992. Hydrogen exchange in native and alcohol forms of ubiquitin. Biochemistry 31:11405-11412.
89. Perrett S, Clarke J, Hounslow AM, Fersht AR. 1995. Relationship between equilibrium amide proton exchange behavior and the folding pathway of barnase. Biochemistry 34:9288-9298.
90. Portman JJ, Takada S, Wolynes PG. 1998. Variational theory for site resolved protein folding free energy surfaces. Phys Rev Lett 81:5231-5240.
91. Radford SE, Buck M, Topping KD, Dobson CM, Evans PA. 1992a. Hydrogen exchange in native and denatured states of hen egg-white lysozyme. Proteins Struct Funct Genet 14:237-248.
92. Radford SE, Dobson CM, Evans PA. 1992b. The folding of hen lysozyme involves partially structured intermediates and multiple pathways. Nature 355:302-307.
93. Raschke TM, Marqusee S. 1997. The kinetic folding intermediate of ribonuclease H resembles the acid molten globule and partially unfolded molecules detected under native conditions. Nature Struct Biol 4:298-304.
94. Robertson AD, Baldwin RL. 1991. Hydrogen exchange in thermally denatured ribonuclease A. Biochemistry 30:9907-9914.
95. Roder H, Elöve GA, Englander SW. 1988. Structural characterization of folding intermediates in cytochrome c by H-exchange labelling and proton NMR. Nature 335:700-704.
96. Roder H, Wüthrich K. 1986. Protein folding kinetics by combined use of rapid mixing techniques and NMR observation of individual amide protons. Proteins Struct Funct Genet 1:34-42.
97. Rosenberg A, Chakravarti K. 1968. Studies of hydrogen exchange in proteins. The exchange kinetics of bovine carbonic anhydrase. J Biol Chem 243:5193-5201.
98. Schönbrunner N, Wey J, Engels J, Georg H, Kiefhaber T. 1996. Native-like β-structure in a trifluoroethanol-induced partially folded state of the all-β-sheet protein tendamistat. J Mol Biol 260:432-445.
99. Schulman BA, Redfield C, Peng Z-Y, Dobson CM, Kim PS. 1995. Different subdomains are most protected from hydrogen exchange in the molten globule and native states of human α-lactalbumin. J Mol Biol 253:651-657.
100. Serrano L, Matouschek A, Fersht AR. 1992. The folding of an enzyme III. Structure of the transition state for unfolding of barnase analyzed by a protein engineering procedure. J Mol Biol 224:805-818.
101. Shoemaker BA, Wang J, Wolynes PG. 1997. Structural correlations in protein folding funnels. Proc Natl Acad Sci USA 94:777-782.
102. Sivaraman T, Kumar TKS, Chang DK, Lin WY, Yu C. 1998. Events in the kinetic folding pathway of a small, all β-sheet protein. J Biol Chem 273:10181-10189.
103. Smith D, Deng Y, Zhang Z. 1997. Probing the non-covalent structure of proteins by amide hydrogen exchange and mass spectrometry. J Mass Spectrom 32:135-146.
104. Sosnick TR, Mayne L, Hiller R, Englander SW. 1994. The barriers in protein folding. Nature Struct Biol 1:149-156.
105. Stockman BJ, Euvrard A, Scahill TA. 1993. Heteronuclear three-dimensional NMR spectroscopy of a partially denatured protein: The A-state of human ubiquitin. J Biomol NMR 3:285-296.
106. Swint-Kruse L, Robertson AD. 1996. Temperature and pH dependences of hydrogen exchange and global stability for ovomucoid third domain. Biochemistry 35:171-180.
107. Thirumalai D, Woodson SA. 1996. Kinetics of folding of proteins and RNA. Acc Chem Res 29:433-439.
108. Tirado-Rives J, Orozco M, Jorgensen WL. 1997. Molecular dynamics simulations of the unfolding of barnase in water and 8 M aqueous urea. Biochemistry 36:7313-7329.
109. Tüchsen E, Woodward C. 1985. Hydrogen exchange kinetics of peptide amide protons at the bovine pancreatic trypsin inhibitor protein-solvent interface. J Mol Biol 185:405-419.
110. Udgaonkar JB, Baldwin RL. 1990. Early folding intermediate of ribonuclease A. Proc Natl Acad Sci USA 87:8197-8201.
111. Varley P, Gronenborn AM, Christensen H, Wingfield PT, Pain RH, Clore GM. 1993. Kinetics of folding of the all-β sheet protein interleukin-1β. Science 260:1110-1113.
112. Walsh ST, Cheng H, Bryson JW, Roder H. DeGrado WF. 1999. Proc Natl Acad Sci USA 11:5486-5491.
113. Wang A, Robertson AD, Bolen DW. 1995. Effects of a naturally occurring compatible osmolyte on the internal dynamics of ribonuclease A. Biochemistry 54:15096-15104.
114. Wang QW, Kline AD, Wüthrich K. 1987. Amide proton exchange in the alpha-amylase polypeptide inhibitor Tendamistat studied by two-dimensional 1H nuclear magnetic resonance. Biochemistry 26:6488-6493.
115. Woodward C. 1993. Is the slow exchange core the protein folding core? Trends Biochem Sci 18:359-360.
116. Woodward C. 1999. Advances in hydrogen exchange from mass spectrometry. J Am Soc Mass Spectrom 10:672-674.
117. Woodward C, Simon I, Tüchsen E. 1982. Hydrogen exchange and the dynamic structure of proteins. Mol Cell Biochem 48:135-160.
118. Woodward CK. 1994. Hydrogen exchange rates and protein folding. Curr Opin Struct Biol 4:112-116.
119. Woodward CK, Hilton BD. 1980. Hydrogen isotope exchange kinetics of single protons in bovine pancreatic trypsin inhibitor. Biophys J 32:561-575.
120. Woodward CK, Rosenberg A. 1971a. Studies of hydrogen exchange in proteins: The correlation of ribonuclease exchange kinetics with the temperature-induced transition. J Biol Chem 246:4105-4113.
121. Woodward CK, Rosenberg A. 1971b. Studies of hydrogen exchange in proteins: Urea effects on ribonuclease exchange kinetics leading to a general model for hydrogen exchange from folded proteins. J Biol Chem 246:4114-4121.
122. Yamasaki K, Ogasahara K, Yutani K, Oobatake M, Kanaya S. 1995. Folding pathway of Escherichia coli ribonuclease HI: A circular dichroism, fluorescence, and NMR study. Biochemistry 34:16552-16562.
123. Yi Q, Baker D. 1996. Direct evidence for a two-state protein unfolding transition from hydrogen-deuterium exchange, mass spectrometry, and NMR. Protein Sci 5:1060-1066.
124. Yi Q, Scalley ML, Simons KT, Gladwin ST, Baker D. 1997. Characterization of the free energy spectrum of peptostreptococcal protein L. Folding Design 2:271-280.
125. 15N assignments and secondary structure of the Src SH3 domain. FEBS Lett 324:87-92.
126. Zhang J, Peng X, Jonas A, Jonas J. 1995. NMR study of the cold, heat and pressure unfolding of ribonuclease A. Biochemistry 34:8631-8641.